Mitochondrial c-Jun N-terminal kinase (JNK) signaling initiates physiological changes resulting in amplification of reactive oxygen species generation

J Biol Chem. 2011 May 6;286(18):16052-62. doi: 10.1074/jbc.M111.223602. Epub 2011 Mar 16.

Abstract

The JNK signaling cascade is critical for cellular responses to a variety of environmental and cellular stimuli. Although gene expression aspects of JNK signal transduction are well studied, there are minimal data on the physiological impact of JNK signaling. To bridge this gap, we investigated how JNK impacted physiology in HeLa cells. We observed that inhibition of JNK activity and JNK silencing with siRNA reduced the level of reactive oxygen species (ROS) generated during anisomycin-induced stress in HeLa cells. Silencing p38 had no significant impact on ROS generation under anisomycin stress. Moreover, JNK signaling mediated amplification of ROS production during stress. Mitochondrial superoxide production was shown to be the source of JNK-induced ROS amplification, as an NADPH oxidase inhibitor demonstrated little impact on JNK-mediated ROS generation. Using mitochondrial isolation from JNK null fibroblasts and targeting the mitochondrial scaffold of JNK, Sab, we demonstrated that mitochondrial JNK signaling was responsible for mitochondrial superoxide amplification. These results suggest that cellular stress altered mitochondria, causing JNK to translocate to the mitochondria and amplify up to 80% of the ROS generated largely by Complex I. This work demonstrates that a sequence of events exist for JNK mitochondrial signaling whereby ROS activates JNK, thereby affecting mitochondrial physiology, which can have effects on cell survival and death.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Anisomycin / pharmacology
  • Electron Transport Complex I / genetics
  • Electron Transport Complex I / metabolism
  • Fibroblasts / cytology
  • Fibroblasts / enzymology*
  • Humans
  • JNK Mitogen-Activated Protein Kinases / genetics
  • JNK Mitogen-Activated Protein Kinases / metabolism*
  • Mice
  • Mice, Knockout
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism*
  • NADPH Oxidases / genetics
  • NADPH Oxidases / metabolism
  • Protein Synthesis Inhibitors / pharmacology
  • Reactive Oxygen Species / metabolism*
  • Signal Transduction / drug effects
  • Signal Transduction / physiology*

Substances

  • Mitochondrial Proteins
  • Protein Synthesis Inhibitors
  • Reactive Oxygen Species
  • Anisomycin
  • NADPH Oxidases
  • JNK Mitogen-Activated Protein Kinases
  • Electron Transport Complex I